Long-term declines in chlorophyll a and variable phenology revealed by a 60-year estuarine plankton time series.

Long-term ecological time series provide a unique perspective on the emergent properties of ecosystems. In aquatic systems, phytoplankton form the base of the food web and their biomass, measured as the concentration of the photosynthetic pigment chlorophyll a (chl a), is an indicator of ecosystem quality. We analyzed temporal trends in chl a from the Long-Term Plankton Time Series in Narragansett Bay, Rhode Island, USA, a temperate estuary experiencing long-term warming and changing anthropogenic nutrient inputs. Dynamic linear models were used to impute and model environmental variables (1959 to 2019) and chl a concentrations (1968 to 2019). A long-term chl a decrease was observed with an average decline in the cumulative annual chl a concentration of 49% and a marked decline of 57% in winter-spring bloom magnitude. The long-term decline in chl a concentration was directly and indirectly associated with multiple environmental factors that are impacted by climate change (e.g., warming temperatures, water column stratification, reduced nutrient concentrations) indicating the importance of accounting for regional climate change effects in ecosystem-based management. Analysis of seasonal phenology revealed that the winter-spring bloom occurred earlier, at a rate of 4.9 ± 2.8 d decade-1. Finally, the high degree of temporal variation in phytoplankton biomass observed in Narragansett Bay appears common among estuaries, coasts, and open oceans. The commonality among these marine ecosystems highlights the need to maintain a robust set of phytoplankton time series in the coming decades to improve signal-to-noise ratios and identify trends in these highly variable environments.

Phytoplankton responses to dust addition in the Fe-Mn co-limited eastern Pacific sub-Antarctic differ by source region.

The seasonal availability of light and micronutrients strongly regulates productivity in the Southern Ocean, restricting biological utilization of macronutrients and CO2 drawdown. Mineral dust flux is a key conduit for micronutrients to the Southern Ocean and a critical mediator of multimillennial-scale atmospheric CO2 oscillations. While the role of dust-borne iron (Fe) in Southern Ocean biogeochemistry has been examined in detail, manganese (Mn) availability is also emerging as a potential driver of past, present, and future Southern Ocean biogeochemistry. Here, we present results from fifteen bioassay experiments along a north-south transect in the undersampled eastern Pacific sub-Antarctic zone. In addition to widespread Fe limitation of phytoplankton photochemical efficiency, we found further responses following the addition of Mn at our southerly stations, supporting the importance of Fe-Mn co-limitation in the Southern Ocean. Moreover, addition of different Patagonian dusts resulted in enhanced photochemical efficiency with differential responses linked to source region dust characteristics in terms of relative Fe/Mn solubility. Changes in the relative magnitude of dust deposition, combined with source region mineralogy, could hence determine whether Fe or Mn limitation control Southern Ocean productivity under future as well as past climate states.

Industrial-era decline in Arctic methanesulfonic acid is offset by increased biogenic sulfate aerosol.

Marine phytoplankton are primary producers in ocean ecosystems and emit dimethyl sulfide (DMS) into the atmosphere. DMS emissions are the largest biological source of atmospheric sulfur and are one of the largest uncertainties in global climate modeling. DMS is oxidized to methanesulfonic acid (MSA), sulfur dioxide, and hydroperoxymethyl thioformate, all of which can be oxidized to sulfate. Ice core records of MSA are used to investigate past DMS emissions but rely on the implicit assumption that the relative yield of oxidation products from DMS remains constant. However, this assumption is uncertain because there are no long-term records that compare MSA to other DMS oxidation products. Here, we share the first long-term record of both MSA and DMS-derived biogenic sulfate concentration in Greenland ice core samples from 1200 to 2006 CE. While MSA declines on average by 0.2 µg S kg-1 over the industrial era, biogenic sulfate from DMS increases by 0.8 µg S kg-1. This increasing biogenic sulfate contradicts previous assertions of declining North Atlantic primary productivity inferred from decreasing MSA concentrations in Greenland ice cores over the industrial era. The changing ratio of MSA to biogenic sulfate suggests that trends in MSA could be caused by time-varying atmospheric chemistry and that MSA concentrations alone should not be used to infer past primary productivity.

A mutant fitness assay identifies bacterial interactions in a model ocean hot spot.

Bacteria that assemble in phycospheres surrounding living phytoplankton cells metabolize a substantial proportion of ocean primary productivity. Yet the type and extent of interactions occurring among species that colonize these micron-scale "hot spot" environments are challenging to study. We identified genes that mediate bacterial interactions in phycosphere communities by culturing a transposon mutant library of copiotrophic bacterium Ruegeria pomeroyi DSS-3 with the diatom Thalassiosira pseudonana CCMP1335 as the sole source of organic matter in the presence or absence of other heterotrophic bacterial species. The function of genes having significant effects on R. pomeroyi fitness indicated explicit cell-cell interactions initiated in the multibacterial phycospheres. We found that R. pomeroyi simultaneously competed for shared substrates while increasing reliance on substrates that did not support the other species' growth. Fitness outcomes also indicated that the bacterium competed for nitrogen in the forms of ammonium and amino acids; obtained purines, pyrimidines, and cofactors via crossfeeding; both initiated and defended antagonistic interactions; and sensed an environment with altered oxygen and superoxide levels. The large genomes characteristic of copiotrophic marine bacteria are hypothesized to enable responses to dynamic ecological challenges occurring at the scale of microns. Here, we discover >200 nonessential genes implicated in the management of fitness costs and benefits of membership in a globally significant bacterial community.

Pumping iron: A multi-omics analysis of two extremophilic algae reveals iron economy management.

Marine algae are responsible for half of the world's primary productivity, but this critical carbon sink is often constrained by insufficient iron. One species of marine algae, Dunaliella tertiolecta, is remarkable for its ability to maintain photosynthesis and thrive in low-iron environments. A related species, Dunaliella salina Bardawil, shares this attribute but is an extremophile found in hypersaline environments. To elucidate how algae manage their iron requirements, we produced high-quality genome assemblies and transcriptomes for both species to serve as a foundation for a comparative multiomics analysis. We identified a host of iron-uptake proteins in both species, including a massive expansion of transferrins and a unique family of siderophore-iron-uptake proteins. Complementing these multiple iron-uptake routes, ferredoxin functions as a large iron reservoir that can be released by induction of flavodoxin. Proteomic analysis revealed reduced investment in the photosynthetic apparatus coupled with remodeling of antenna proteins by dramatic iron-deficiency induction of TIDI1, which is closely related but identifiably distinct from the chlorophyll binding protein, LHCA3. These combinatorial iron scavenging and sparing strategies make Dunaliella unique among photosynthetic organisms.

The adaptive mechanisms of the marine diatom Thalassiosira weissflogii to long-term high CO2 and warming.

While it is known that increased dissolved CO2 concentrations and rising sea surface temperature (ocean warming) can act interactively on marine phytoplankton, the ultimate molecular mechanisms underlying this interaction on a long-term evolutionary scale are relatively unexplored. Here, we performed transcriptomics and quantitative metabolomics analyses, along with a physiological trait analysis, on the marine diatom Thalassiosira weissflogii adapted for approximately 3.5 years to warming and/or high CO2 conditions. We show that long-term warming has more pronounced impacts than elevated CO2 on gene expression, resulting in a greater number of differentially expressed genes (DEGs). The largest number of DEGs was observed in populations adapted to warming + high CO2, indicating a potential synergistic interaction between these factors. We further identified the metabolic pathways in which the DEGs function and the metabolites with significantly changed abundances. We found that ribosome biosynthesis-related pathways were upregulated to meet the increased material and energy demands after warming or warming in combination with high CO2. This resulted in the upregulation of energy metabolism pathways such as glycolysis, photorespiration, the tricarboxylic acid cycle, and the oxidative pentose phosphate pathway, as well as the associated metabolites. These metabolic changes help compensate for reduced photochemical efficiency and photosynthesis. Our study emphasizes that the upregulation of ribosome biosynthesis plays an essential role in facilitating the adaptation of phytoplankton to global ocean changes and elucidates the interactive effects of warming and high CO2 on the adaptation of marine phytoplankton in the context of global change.

Space, the final frontier: The spatial component of phytoplankton-bacterial interactions.

Microscale interactions between marine phytoplankton and bacteria shape the microenvironment of individual cells, impacting their physiology and ultimately influencing global-scale biogeochemical processes like carbon and nutrient cycling. In dilute environments such as the ocean water column, metabolic exchange between microorganisms likely requires close proximity between partners. However, the biological strategies to achieve this physical proximity remain an understudied aspect of phytoplankton-bacterial associations. Understanding the mechanisms by which these microorganisms establish and sustain spatial relationships and the extent to which spatial proximity is necessary for interactions to occur, is critical to learning how spatial associations influence the ecology of phytoplankton and bacterial communities. Here, we provide an overview of current knowledge on the role of space in shaping interactions among ocean microorganisms, encompassing behavioural and metabolic evidence. We propose that characterising phytoplankton-bacterial interactions from a spatial perspective can contribute to a mechanistic understanding of the establishment and maintenance of these associations and, consequently, an enhanced ability to predict the impact of microscale processes on ecosystem-wide phenomena.

Estimation of functional diversity and species traits from ecological monitoring data.

The twin crises of climate change and biodiversity loss define a strong need for functional diversity monitoring. While the availability of high-quality ecological monitoring data is increasing, the quantification of functional diversity so far requires the identification of species traits, for which data are harder to obtain. However, the traits that are relevant for the ecological function of a species also shape its performance in the environment and hence, should be reflected indirectly in its spatiotemporal distribution. Thus, it may be possible to reconstruct these traits from a sufficiently extensive monitoring dataset. Here, we use diffusion maps, a deterministic and de facto parameter-free analysis method, to reconstruct a proxy representation of the species' traits directly from monitoring data and use it to estimate functional diversity. We demonstrate this approach with both simulated data and real-world phytoplankton monitoring data from the Baltic Sea. We anticipate that wider application of this approach to existing data could greatly advance the analysis of changes in functional biodiversity.

Elongation enhances encounter rates between phytoplankton in turbulence.

Phytoplankton come in a stunning variety of shapes but elongated morphologies dominate-typically 50% of species have aspect ratio above 5, and bloom-forming species often form chains whose aspect ratios can exceed 100. How elongation affects encounter rates between phytoplankton in turbulence has remained unknown, yet encounters control the formation of marine snow in the ocean. Here, we present simulations of encounters among elongated phytoplankton in turbulence, showing that encounter rates between neutrally buoyant elongated cells are up to 10-fold higher than for spherical cells and even higher when cells sink. Consequently, we predict that elongation can significantly speed up the formation of marine snow compared to spherical cells. This unexpectedly large effect of morphology in driving encounter rates among plankton provides a potential mechanistic explanation for the rapid clearance of many phytoplankton blooms.

Environmental control of marine phytoplankton stoichiometry in the North Atlantic Ocean.

The stoichiometric coupling of carbon to limiting nutrients in marine phytoplankton regulates the magnitude of biological carbon sequestration in the ocean. While clear links between plankton C:N ratios and environmental drivers have been identified, the nature and direction of these links, as well as their underlying physiological and ecological controls, remain uncertain. We show, with a well-constrained mechanistic model of plankton ecophysiology, that while nitrogen availability and temperature emerge as the main drivers of phytoplankton C:N stoichiometry in the North Atlantic, the biological mechanisms involved vary depending on the spatiotemporal scale and region considered. We find that phytoplankton C:N stoichiometry is overall controlled by nitrogen availability below 40° N, predominantly driven by ecoevolutionary shifts in the functional composition of the phytoplankton communities, while phytoplankton stoichiometric plasticity in response to dropping temperatures and increased grazing pressure dominates at higher latitudes. Our findings highlight the potential of "organisms-to-ecosystems" modeling approaches based on mechanistic models of plankton biology accounting for physiology, ecology, and trait evolution to explore and explain complex observational data and ultimately improve the predictions of global ocean models.

The dimensionality of infection networks among viruses infecting microbial eukaryotes and bacteria.

Diverse viruses and their hosts are interconnected through complex networks of infection, which are thought to influence ecological and evolutionary processes, but the principles underlying infection network structure are not well understood. Here we focus on network dimensionality and how it varies across 37 networks of viruses infecting eukaryotic phytoplankton and bacteria. We find that dimensionality is often strikingly low, with most networks being one- or two-dimensional, although dimensionality increases with network richness, suggesting that the true dimensionality of natural systems is higher. Low-dimensional networks generally exhibit a mixture of host partitioning among viruses and nestededness of host ranges. Networks of bacteria-infecting and eukaryote-infecting viruses possess comparable distributions of dimensionality and prevalence of nestedness, indicating that fundamentals of network structure are similar among domains of life and different viral lineages. The relative simplicity of many infection networks suggests that coevolutionary dynamics are often driven by a modest number of underlying mechanisms.

Interactions between temperature and nutrients determine the population dynamics of primary producers.

Global change is rapidly and fundamentally altering many of the processes regulating the flux of energy throughout ecosystems, and although researchers now understand the effect of temperature on key rates (such as aquatic primary productivity), the theoretical foundation needed to generate forecasts of biomass dynamics and extinction risk remains underdeveloped. We develop new theory that describes the interconnected effects of nutrients and temperature on phytoplankton populations and show that the thermal response of equilibrium biomass (i.e. carrying capacity) always peaks at a lower temperature than for productivity (i.e. growth rate). This mismatch is driven by differences in the thermal responses of growth, death, and per-capita impact on the nutrient pool, making our results highly general and applicable to widely used population models beyond phytoplankton. We further show that non-equilibrium dynamics depend on the pace of environmental change relative to underlying vital rates and that populations respond to variable environments differently at high versus low temperatures due to thermal asymmetries.

Multi-trait diversification in marine diatoms in constant and warmed environments.

Phytoplankton are photosynthetic marine microbes that affect food webs, nutrient cycles and climate regulation. Their roles are determined by correlated phytoplankton functional traits including cell size, chlorophyll content and cellular composition. Here, we explore patterns of evolution in interrelated trait values and correlations. Because both chance events and natural selection contribute to phytoplankton trait evolution, we used population bottlenecks to diversify six genotypes of Thalassiosirid diatoms. We then evolved them as large populations in two environments. Interspecific variation and within-species evolution were visualized for nine traits and their correlations using reduced axes (a trait-scape). Our main findings are that shifts in trait values resulted in movement of evolving populations within the trait-scape in both environments, but were more frequent when large populations evolved in a novel environment. Which trait relationships evolved was population-specific, but greater departures from ancestral trait correlations were associated with lower population growth rates. There was no single master trait that could be used to understand multi-trait evolution. Instead, repeatable multi-trait evolution occurred along a major axis of variation defined by several diatom traits and trait relationships. Because trait-scapes capture changes in trait relationships and values together, they offer an insightful way to study multi-trait variation.

The enhanced neutral process with decreasing cell size: a study on phytoplankton metacommunities from the glacier-fed river of Qinghai-Xizang Plateau.

The cell size of phytoplankton is an important defining functional trait that can serve as a driver and sentinel of phytoplankton community structure and function. However, the study of the assembly patterns and drivers of phytoplankton metacommunities with different cell sizes has not been widely carried out. In this study, we systematically investigated the biodiversity patterns, drivers, and assembly processes of the three phytoplankton cell sizes (micro: 20-200 µm; nano: 2-20 µm; pico: 0.2-2 µm) in the Za'gya Zangbo River from the source to the estuary using 18S rDNA amplicon sequencing. The results demonstrated that the alpha diversity and co-occurrence network complexity for all three sizes of phytoplankton increased to a peak downstream of the glacier sources and then decreased to the estuary. The nanophytoplankton subcommunity consistently had the highest alpha diversity and co-occurrence network complexity. On the other hand, total beta diversity followed a unimodal trend of decreasing and then increasing from source to estuary, and was dominated by species replacement components. In addition, deterministic processes driven mainly by physiochemical indices (PCIs) and biogenic elements (BGEs) dominated the assembly of micro- and nanophytoplankton subcommunities, whereas stochastic processes driven by geographical factors (GGFs) dominated the assembly of picophytoplankton subcommunities. The results explained the contradictions in previous studies of phytoplankton community assembly processes in highland aquatic ecosystems, elucidating the different contributions of deterministic and stochastic processes, and the complexity of compositional mechanisms in shaping the assembly of micro-, nano-, and picophytoplankton in this highland glacial river. IMPORTANCE: The cell size of phytoplankton is a key life-history trait and key determinant, and phytoplankton of different cell sizes are differentially affected by ecological processes. However, the study of the assembly patterns and drivers of phytoplankton metacommunities with different cell sizes has not been widely carried out. We provide an in-depth analysis of phytoplankton community diversity across three cell sizes in the glacier-fed river, describing how the pattern of phytoplankton communities differs across cell sizes in response to geochemical gradients. The results show that the smaller phytoplankton (picophytoplankton) are relatively more influenced by dispersal-based stochastic processes, whereas larger ones (microphytoplankton and nanophytoplankton) are more structured by selection-based deterministic processes.

Stimulating and toxic effect of chromium on growth and photosynthesis of a marine chlorophyte.

Marine phytoplankton can interchange trace metals in various biochemical functions, particularly under metal-limiting conditions. Here, we investigate the stimulating and toxicity effect of chromium (Cr) on a marine Chlorophyceae Osetreococcus tauri under Fe-replete and Fe-deficient conditions. We determined the growth, photosynthesis, and proteome expressions of Osetreococcus tauri cultured under different Cr and Fe concentrations. In Fe-replete conditions, the presence of Cr(VI) stimulated significantly the growth rate and the maximum yield of photochemistry of photosystem II (Fv /Fm ) of the phytoplankton, while the functional absorption cross-section of photosystem II (σPSII ) did not change. Minor additions of Cr(VI) partially rescued phytoplankton growth under Fe-limited conditions. Proteomic analysis of this alga grown in Fe-replete normal and Fe-replete with Cr addition media (10 µM Cr) showed that the presence of Cr significantly decreased the expression of phosphate-transporting proteins and photosynthetic proteins, while increasing the expression of proteins related to carbon assimilation. Cr can stimulate the growth and photosynthesis of O. tauri, but the effects are dependent on both the Cr(VI) concentration and the availability of Fe. The proteomic results further suggest that Cr(VI) addition might significantly increase starch production and carbon fixation.

Inter-algal associations and nutrients linked by Scenedesmus and Desmodesmus structure eukaryotic algal communities.

Eutrophication reduces the variability of the community composition of plankton. However, the mechanisms underlying the diversity and restructuring of eukaryotic algal communities remain unknown. This study analysed the diversity and compositional patterns of algal communities in shallow eutrophic lakes. It investigated how these communities were modified by key genera through mediating inter-algal associations under the influence of abiotic factors. Inter-algal associations explained more variance in algal communities than environmental variables, and variation in composition and diversity was primarily derived from Scenedesmus, Desmodesmus and Cryptomonas, rather than nutrients. Scenedesmus and Desmodesmus were positively correlated with the genera of Chlorophyta and formed the hub of the algal association network. When the relative abundance of Scenedesmus and Desmodesmus increased from 0.41% to 13.74%, communities enriched in biomarkers of Bacillariophyta, Chrysophyceae and Cryptophyta transitioned to communities enriched in biomarkers of Chlorophyta. Moreover, negative associations between the Chlorophyta hub genera and other non-Chlorophyta genera increased. High concentrations of total phosphorus altered the composition of algal communities by increasing the abundance of Scenedesmus and Desmodesmus, which in turn had cascading effects through inter-algal associations. Additionally, algal communities with higher abundances of Scenedesmus and Desmodesmus were more susceptible to the effects of total phosphorus. Our study suggested that inter-algal associations, centred on Scenedesmus and Desmodesmus, had a greater influence on algal diversity and community structure than other factors. Nutrient levels were not a direct driver of algal diversity and community structure adjustments, but acted indirectly by enhancing the influence of Scenedesmus and Desmodesmus.

Using picosecond fluorescence lifetime analysis to determine photosynthesis in the world's oceans.

Phytoplankton in the ocean account for less than 1% of the global photosynthetic biomass, but contribute about 45% of the photosynthetically fixed carbon on Earth. This amazing production/biomass ratio implies a very high photosynthetic efficiency. But, how efficiently is the absorbed light used in marine photosynthesis? The introduction of picosecond and then femtosecond lasers for kinetic measurements in mid 1970s to 90 s was a revolution in basic photosynthesis research that vastly improved our understanding of the energy conversion processes in photosynthetic reactions. Until recently, the use of this technology in the ocean was not feasible due to the complexity of related instrumentation and the lack of picosecond lasers suitable for routine operation in the field. However, recent advances in solid-state laser technology and the development of compact data acquisition electronics led to the application of picosecond fluorescence lifetime analyses in the field. Here, we review the development of operational ultrasensitive picosecond fluorescence instruments to infer photosynthetic energy conversion processes in ocean ecosystems. This analysis revealed that, in spite of the high production/biomass ratio in marine phytoplankton, the photosynthetic energy conversion efficiency is exceptionally low-on average, ca. 50% of its maximum potential, suggesting that most of the contemporary open ocean surface waters are extremely nutrient deficient.

Diversity, Genomics, and Distribution of Phytoplankton-Cyanobacterium Single-Cell Symbiotic Associations.

Cyanobacteria are common in symbiotic relationships with diverse multicellular organisms (animals, plants, fungi) in terrestrial environments and with single-celled heterotrophic, mixotrophic, and autotrophic protists in aquatic environments. In the sunlit zones of aquatic environments, diverse cyanobacterial symbioses exist with autotrophic taxa in phytoplankton, including dinoflagellates, diatoms, and haptophytes (prymnesiophytes). Phototrophic unicellular cyanobacteria related to Synechococcus and Prochlorococcus are associated with a number of groups. N2-fixing cyanobacteria are symbiotic with diatoms and haptophytes. Extensive genome reduction is involved in the N2-fixing endosymbionts, most dramatically in the unicellular cyanobacteria associated with haptophytes, which have lost most of the photosynthetic apparatus, the ability to fix C, and the tricarboxylic acid cycle. The mechanisms involved in N2-fixing symbioses may involve more interactions beyond simple exchange of fixed C for N. N2-fixing cyanobacterial symbioses are widespread in the oceans, even more widely distributed than the best-known free-living N2-fixing cyanobacteria, suggesting they may be equally or more important in the global ocean biogeochemical cycle of N.Despite their ubiquitous nature and significance in biogeochemical cycles, cyanobacterium-phytoplankton symbioses remain understudied and poorly understood.

Land use change and coastal water darkening drive synchronous dynamics in phytoplankton and fish phenology on centennial timescales.

At high latitudes, the suitable window for timing reproductive events is particularly narrow, promoting tight synchrony between trophic levels. Climate change may disrupt this synchrony due to diverging responses to temperature between, for example, the early life stages of higher trophic levels and their food resources. Evidence for this is equivocal, and the role of compensatory mechanisms is poorly understood. Here, we show how a combination of ocean warming and coastal water darkening drive long-term changes in phytoplankton spring bloom timing in Lofoten Norway, and how spawning time of Northeast Arctic cod responds in synchrony. Spring bloom timing was derived from hydrographical observations dating back to 1936, while cod spawning time was estimated from weekly fisheries catch and roe landing data since 1877. Our results suggest that land use change and freshwater run-off causing coastal water darkening has gradually delayed the spring bloom up to the late 1980s after which ocean warming has caused it to advance. The cod appear to track phytoplankton dynamics by timing gonadal development and spawning to maximize overlap between offspring hatch date and predicted resource availability. This finding emphasises the importance of land-ocean coupling for coastal ecosystem functioning, and the potential for fish to adapt through phenotypic plasticity.

Long-term studies on West Antarctic Peninsula phytoplankton blooms suggest range shifts between temperate and polar species.

The Western Antarctic Peninsula (WAP) experiences one of the highest rates of sea surface warming globally, leading to potential changes in biological communities. Long-term phytoplankton monitoring in Potter Cove (PC, King George Island, South Shetlands) from the 1990s to 2009 revealed consistently low biomass values, and sporadic blooms dominated by cold-water microplankton diatoms. However, a significant change occurred between 2010 and 2020, marked by a notable increase in intense phytoplankton blooms in the region. During this period, the presence of a nanoplankton diatom, Shionodiscus gaarderae, was documented for the first time. In some instances, this species even dominated the blooms. S. gaarderae is recognized for producing blooms in temperate waters in both hemispheres. However, its blooming in the northern Southern Ocean may suggest either a recent introduction or a range shift associated with rising temperatures in the WAP, a phenomenon previously observed in experimental studies. The presence of S. gaarderae could be viewed as a warning sign of significant changes already underway in the northern WAP plankton communities. This includes the potential replacement of microplankton diatoms by smaller nanoplankton species. This study, based on observations along the past decade, and compared to the previous 20 years, could have far-reaching implications for the structure of the Antarctic food web.